Environmental and biotic controls on the evolutionary history of insect body size

Abstract

Giant insects, with wingspans as large as 70 cm, ruled the Carboniferous and Permian skies. Gigantism has been linked to hyperoxic conditions because oxygen concentration is a key physiological control on body size, particularly in groups like flying insects that have high metabolic oxygen demands. Here we show, using a dataset of more than 10,500 fossil insect wing lengths, that size tracked atmospheric oxygen concentrations only for the first 150 Myr of insect evolution. The data are best explained by a model relating maximum size to atmospheric environmental oxygen concentration (pO(2)) until the end of the Jurassic, and then at constant sizes, independent of oxygen fluctuations, during the Cretaceous and, at a smaller size, the Cenozoic. Maximum insect size decreased even as atmospheric pO(2) rose in the Early Cretaceous following the evolution and radiation of early birds, particularly as birds acquired adaptations that allowed more agile flight. A further decrease in maximum size during the Cenozoic may relate to the evolution of bats, the Cretaceous mass extinction, or further specialization of flying birds. The decoupling of insect size and atmospheric pO(2) coincident with the radiation of birds suggests that biotic interactions, such as predation and competition, superseded oxygen as the most important constraint on maximum body size of the largest insects.

Fig. 1.

Phanerozoic trends in insect wing lengths and atmospheric pO₂ (GEOCARBSULF model). Maximum size in each 10-Myr bin containing more than 50 measurements is indicated by black lines.

Fig. 2.

Maximum-likelihood model fit relative to timing of shift from atmospheric pO₂ control to size stasis. (A) Log-likelihood plotted against all possible breakpoints in a two-phase size evolution model. Greater log-likelihoods indicate greater support for a breakpoint, implying that the best breakpoint is at 140–130 Ma. (B) Log-likelihood contours on all possible two-breakpoint combinations in a three-phase size evolution model (breakpoints must be separated by three intervals to fit the models). The best-supported pair of breakpoints is at 140–130 Ma and 90–60 Ma. The support for a 270–260 Ma breakpoint is an artifact of the shift from extremely insect-rich bins to insect-poor Late Permian bins.